Selective Recruitment of Nuclear Factors to Productively Replicating Herpes Simplex Virus Genomes

English version České info

HSV-1 is a human pathogen that infects over 50% of the population. The virus persists as a latent infection in the ganglia of an infected host and upon stressful conditions is reactivated to a lytic state in which it causes recurrent sores at the initial site of infection. During lytic infection, HSV highjacks the host cell to propagate its genome and produce new virus particles. However, there is limited knowledge of what cellular proteins interact with and function on the viral genome. We therefore developed methods to purify viral genomes from productively infected cells to identify associated viral and cellular proteins. We found proteins and protein complexes that have previously been implicated in HSV infection to be enriched on viral genomes, as well as several novel proteins that are likely involved in productive infection. These data provide valuable insight into HSV biology. Furthermore, these methods can be adapted to study other viruses, as well as other aspects of the HSV life cycle.

Vyšlo v časopise: Selective Recruitment of Nuclear Factors to Productively Replicating Herpes Simplex Virus Genomes. PLoS Pathog 11(5): e32767. doi:10.1371/journal.ppat.1004939
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004939

Souhrn

Zdroje

1. McGeoch DJ, Dalrymple MA, Davison AJ, Dolan A, Frame MC, et al. (1988) The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1. J Gen Virol 69: 1531–1574. 2839594

2. McGeoch DJ, Dolan A, Donald S, Brauer DH (1986) Complete DNA sequence of the short repeat region in the genome of herpes simplex virus type 1. Nucleic Acids Res 14: 1727–1745. 3005980

3. Batterson W, Furlong D, Roizman B (1983) Molecular genetics of herpes simplex virus. VIII. further characterization of a temperature-sensitive mutant defective in release of viral DNA and in other stages of the viral reproductive cycle. J Virol 45: 397–407. 6296445

4. Ojala PM, Sodeik B, Ebersold MW, Kutay U, Helenius A (2000) Herpes simplex virus type 1 entry into host cells: reconstitution of capsid binding and uncoating at the nuclear pore complex in vitro. Mol Cell Biol 20: 4922–4931. 10848617

5. Shahin V, Hafezi W, Oberleithner H, Ludwig Y, Windoffer B, et al. (2006) The genome of HSV-1 translocates through the nuclear pore as a condensed rod-like structure. J Cell Sci 119: 23–30. 16339172

6. Maul GG (1998) Nuclear domain 10, the site of DNA virus transcription and replication. Bioessays 20: 660–667. 9780840

7. Smith S, Reuven N, Mohni KN, Schumacher AJ, Weller SK (2014) Structure of the herpes simplex virus 1 genome: manipulation of nicks and gaps can abrogate infectivity and alter the cellular DNA damage response. J Virol 88: 10146–10156. doi: 10.1128/JVI.01723-14 24965466

8. Everett RD (2001) DNA viruses and viral proteins that interact with PML nuclear bodies. Oncogene 20: 7266–7273. 11704855

9. Taylor TJ, McNamee EE, Day C, Knipe DM (2003) Herpes simplex virus replication compartments can form by coalescence of smaller compartments. Virology 309: 232–247. 12758171

10. Batterson W, Roizman B (1983) Characterization of the herpes simplex virion-associated factor responsible for the induction of alpha genes. J Virol 46: 371–377. 6302308

11. Campbell ME, Palfreyman JW, Preston CM (1984) Identification of herpes simplex virus DNA sequences which encode a trans-acting polypeptide responsible for stimulation of immediate early transcription. J Mol Biol 180: 1–19. 6096556

12. Watson RJ, Clements JB (1980) A herpes simplex virus type 1 function continuously required for early and late virus RNA synthesis. Nature 285: 329–330. 6246451

13. Alwine JC, Steinhart WL, Hill CW (1974) Transcription of herpes simplex type 1 DNA in nuclei isolated from infected HEp-2 and KB cells. Virology 60: 302–307. 4366499

14. Everett RD, Sourvinos G, Orr A (2003) Recruitment of herpes simplex virus type 1 transcriptional regulatory protein ICP4 into foci juxtaposed to ND10 in live, infected cells. J Virol 77: 3680–3689. 12610143

15. Everett RD, Sourvinos G, Leiper C, Clements JB, Orr A (2004) Formation of nuclear foci of the herpes simplex virus type 1 regulatory protein ICP4 at early times of infection: localization, dynamics, recruitment of ICP27, and evidence for the de novo induction of ND10-like complexes. J Virol 78: 1903–1917. 14747555

16. La Boissiere S, Izeta A, Malcomber S, O'Hare P (2004) Compartmentalization of VP16 in cells infected with recombinant herpes simplex virus expressing VP16-green fluorescent protein fusion proteins. J Virol 78: 8002–8014. 15254172

17. Honess RW, Roizman B (1974) Regulation of herpesvirus macromolecular synthesis. I. Cascade regulation of the synthesis of three groups of viral proteins. J Virol 14: 8–19. 4365321

18. Honess RW, Roizman B (1975) Regulation of herpesvirus macromolecular synthesis: sequential transition of polypeptide synthesis requires functional viral polypeptides. Proc Natl Acad Sci U S A 72: 1276–1280. 165503

19. Challberg MD (1986) A method for identifying the viral genes required for herpesvirus DNA replication. Proc Natl Acad Sci U S A 83: 9094–9098. 3024166

20. Weller SK, Coen DM (2012) Herpes simplex viruses: mechanisms of DNA replication. Cold Spring Harb Perspect Biol 4: a013011. doi: 10.1101/cshperspect.a013011 22952399

21. Cardone G, Heymann JB, Cheng N, Trus BL, Steven AC (2012) Procapsid assembly, maturation, nuclear exit: dynamic steps in the production of infectious herpesvirions. Adv Exp Med Biol 726: 423–439. doi: 10.1007/978-1-4614-0980-9_19 22297525

22. Wang IH, Suomalainen M, Andriasyan V, Kilcher S, Mercer J, et al. (2013) Tracking viral genomes in host cells at single-molecule resolution. Cell Host Microbe 14: 468–480. doi: 10.1016/j.chom.2013.09.004 24139403

23. Sirbu BM, McDonald WH, Dungrawala H, Badu-Nkansah A, Kavanaugh GM, et al. (2013) Identification of proteins at active, stalled, and collapsed replication forks using isolation of proteins on nascent DNA (iPOND) coupled with mass spectrometry. J Biol Chem 288: 31458–31467. doi: 10.1074/jbc.M113.511337 24047897

24. Sirbu BM, Couch FB, Feigerle JT, Bhaskara S, Hiebert SW, et al. (2011) Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev 25: 1320–1327. doi: 10.1101/gad.2053211 21685366

25. Sirbu BM, Couch FB, Cortez D (2012) Monitoring the spatiotemporal dynamics of proteins at replication forks and in assembled chromatin using isolation of proteins on nascent DNA. Nat Protoc 7: 594–605. doi: 10.1038/nprot.2012.010 22383038

26. Lopez-Contreras AJ, Ruppen I, Nieto-Soler M, Murga M, Rodriguez-Acebes S, et al. (2013) A proteomic characterization of factors enriched at nascent DNA molecules. Cell Rep 3: 1105–1116. doi: 10.1016/j.celrep.2013.03.009 23545495

27. Dungrawala H, Cortez D (2015) Purification of proteins on newly synthesized DNA using iPOND. Methods Mol Biol 1228: 123–131. doi: 10.1007/978-1-4939-1680-1_10 25311126

28. Aranda S, Rutishauser D, Ernfors P (2014) Identification of a large protein network involved in epigenetic transmission in replicating DNA of embryonic stem cells. Nucleic Acids Res 42: 6972–6986. doi: 10.1093/nar/gku374 24852249

29. Everett RD, Murray J, Orr A, Preston CM (2007) Herpes simplex virus type 1 genomes are associated with ND10 nuclear substructures in quiescently infected human fibroblasts. J Virol 81: 10991–11004. 17670833

30. Hobbs WE, DeLuca NA (1999) Perturbation of cell cycle progression and cellular gene expression as a function of herpes simplex virus ICP0. Journal of Virology 73: 8245–8255. 10482575

31. Lomonte P, Everett RD (1999) Herpes simplex virus type 1 immediate-early protein Vmw110 inhibits progression of cells through mitosis and from G(1) into S phase of the cell cycle. J Virol 73: 9456–9467. 10516054

32. Haug T, Skorpen F, Aas PA, Malm V, Skjelbred C, et al. (1998) Regulation of expression of nuclear and mitochondrial forms of human uracil-DNA glycosylase. Nucleic Acids Res 26: 1449–1457. 9490791

33. Leung KH, Abou El Hassan M, Bremner R (2013) A rapid and efficient method to purify proteins at replication forks under native conditions. Biotechniques 55: 204–206. doi: 10.2144/000114089 24107252

34. Wagner LM, DeLuca NA (2013) Temporal association of herpes simplex virus ICP4 with cellular complexes functioning at multiple steps in PolII transcription. PLoS One 8: e78242. doi: 10.1371/journal.pone.0078242 24147125

35. Lester JT, DeLuca NA (2011) Herpes simplex virus 1 ICP4 forms complexes with TFIID and mediator in virus-infected cells. J Virol 85: 5733–5744. doi: 10.1128/JVI.00385-11 21450820

36. Mellacheruvu D, Wright Z, Couzens AL, Lambert JP, St-Denis NA, et al. (2013) The CRAPome: a contaminant repository for affinity purification-mass spectrometry data. Nat Methods 10: 730–736. doi: 10.1038/nmeth.2557 23921808

37. Leinbach SS, Summers WC (1980) The structure of herpes simplex virus type 1 DNA as probed by micrococcal nuclease digestion. J Gen Virol 51: 45–59. 6257837

38. Mouttet ME, Guetard D, Bechet JM (1979) Random cleavage of intranuclear herpes simplex virus DNA by micrococcal nuclease. FEBS Lett 100: 107–109. 220083

39. Oh J, Fraser NW (2008) Temporal association of the herpes simplex virus genome with histone proteins during a lytic infection. J Virol 82: 3530–3537. 18160436

40. Kent JR, Zeng PY, Atanasiu D, Gardner J, Fraser NW, et al. (2004) During lytic infection herpes simplex virus type 1 is associated with histones bearing modifications that correlate with active transcription. J Virol 78: 10178–10186. 15331750

41. Huang J, Kent JR, Placek B, Whelan KA, Hollow CM, et al. (2006) Trimethylation of histone H3 lysine 4 by Set1 in the lytic infection of human herpes simplex virus 1. J Virol 80: 5740–5746. 16731913

42. Deshmane SL, Fraser NW (1989) During latency, herpes simplex virus type 1 DNA is associated with nucleosomes in a chromatin structure. J Virol 63: 943–947. 2536115

43. Capranico G, Marinello J, Baranello L (2010) Dissecting the transcriptional functions of human DNA topoisomerase I by selective inhibitors: implications for physiological and therapeutic modulation of enzyme activity. Biochim Biophys Acta 1806: 240–250. doi: 10.1016/j.bbcan.2010.06.003 20600630

44. Wilcock D, Lane DP (1991) Localization of p53, retinoblastoma and host replication proteins at sites of viral replication in herpes-infected cells. Nature 349: 429–431. 1671528

45. Taylor TJ, Knipe DM (2004) Proteomics of herpes simplex virus replication compartments: association of cellular DNA replication, repair, recombination, and chromatin remodeling proteins with ICP8. J Virol 78: 5856–5866. 15140983

46. Lilley CE, Carson CT, Muotri AR, Gage FH, Weitzman MD (2005) DNA repair proteins affect the lifecycle of herpes simplex virus 1. Proc Natl Acad Sci U S A 102: 5844–5849. 15824307

47. Shirata N, Kudoh A, Daikoku T, Tatsumi Y, Fujita M, et al. (2005) Activation of ataxia telangiectasia-mutated DNA damage checkpoint signal transduction elicited by herpes simplex virus infection. J Biol Chem 280: 30336–30341. 15964848

48. Lilley CE, Schwartz RA, Weitzman MD (2007) Using or abusing: viruses and the cellular DNA damage response. Trends Microbiol 15: 119–126. 17275307

49. Lilley CE, Chaurushiya MS, Boutell C, Landry S, Suh J, et al. (2010) A viral E3 ligase targets RNF8 and RNF168 to control histone ubiquitination and DNA damage responses. EMBO J 29: 943–955. doi: 10.1038/emboj.2009.400 20075863

50. Parkinson J, Lees-Miller SP, Everett RD (1999) Herpes simplex virus type 1 immediate-early protein vmw110 induces the proteasome-dependent degradation of the catalytic subunit of DNA-dependent protein kinase. J Virol 73: 650–657. 9847370

51. Lilley CE, Chaurushiya MS, Boutell C, Everett RD, Weitzman MD (2011) The intrinsic antiviral defense to incoming HSV-1 genomes includes specific DNA repair proteins and is counteracted by the viral protein ICP0. PLoS Pathog 7: e1002084. doi: 10.1371/journal.ppat.1002084 21698222

52. Wilkinson DE, Weller SK (2003) The role of DNA recombination in herpes simplex virus DNA replication. IUBMB Life 55: 451–458. 14609200

53. Schumacher AJ, Mohni KN, Kan Y, Hendrickson EA, Stark JM, et al. (2012) The HSV-1 exonuclease, UL12, stimulates recombination by a single strand annealing mechanism. PLoS Pathog 8: e1002862. doi: 10.1371/journal.ppat.1002862 22912580

54. Balasubramanian N, Bai P, Buchek G, Korza G, Weller SK (2010) Physical interaction between the herpes simplex virus type 1 exonuclease, UL12, and the DNA double-strand break-sensing MRN complex. J Virol 84: 12504–12514. doi: 10.1128/JVI.01506-10 20943970

55. Hirano T (2005) SMC proteins and chromosome mechanics: from bacteria to humans. Philos Trans R Soc Lond B Biol Sci 360: 507–514. 15897176

56. Mehta GD, Kumar R, Srivastava S, Ghosh SK (2013) Cohesin: functions beyond sister chromatid cohesion. FEBS Lett 587: 2299–2312. doi: 10.1016/j.febslet.2013.06.035 23831059

57. Chen HS, Martin KA, Lu F, Lupey LN, Mueller JM, et al. (2014) Epigenetic deregulation of the LMP1/LMP2 locus of Epstein-Barr virus by mutation of a single CTCF-cohesin binding site. J Virol 88: 1703–1713. doi: 10.1128/JVI.02209-13 24257606

58. Holdorf MM, Cooper SB, Yamamoto KR, Miranda JJ (2011) Occupancy of chromatin organizers in the Epstein-Barr virus genome. Virology 415: 1–5. doi: 10.1016/j.virol.2011.04.004 21550623

59. Mohni KN, Mastrocola AS, Bai P, Weller SK, Heinen CD (2011) DNA mismatch repair proteins are required for efficient herpes simplex virus 1 replication. J Virol 85: 12241–12253. doi: 10.1128/JVI.05487-11 21957315

60. Mullaney J, Moss HW, McGeoch DJ (1989) Gene UL2 of herpes simplex virus type 1 encodes a uracil-DNA glycosylase. J Gen Virol 70 (Pt 2): 449–454. 2567340

61. Sandri-Goldin RM (2011) The many roles of the highly interactive HSV protein ICP27, a key regulator of infection. Future Microbiol 6: 1261–1277. doi: 10.2217/fmb.11.119 22082288

62. Chen IH, Li L, Silva L, Sandri-Goldin RM (2005) ICP27 recruits Aly/REF but not TAP/NXF1 to herpes simplex virus type 1 transcription sites although TAP/NXF1 is required for ICP27 export. J Virol 79: 3949–3961. 15767397

63. Chen IH, Sciabica KS, Sandri-Goldin RM (2002) ICP27 interacts with the RNA export factor Aly/REF to direct herpes simplex virus type 1 intronless mRNAs to the TAP export pathway. J Virol 76: 12877–12889. 12438613

64. Boyne JR, Colgan KJ, Whitehouse A (2008) Recruitment of the complete hTREX complex is required for Kaposi's sarcoma-associated herpesvirus intronless mRNA nuclear export and virus replication. PLoS Pathog 4: e1000194. doi: 10.1371/journal.ppat.1000194 18974867

65. Montes M, Becerra S, Sanchez-Alvarez M, Sune C (2012) Functional coupling of transcription and splicing. Gene 501: 104–117. doi: 10.1016/j.gene.2012.04.006 22537677

66. Pandit S, Wang D, Fu XD (2008) Functional integration of transcriptional and RNA processing machineries. Curr Opin Cell Biol 20: 260–265. doi: 10.1016/j.ceb.2008.03.001 18436438

67. Luna R, Gaillard H, Gonzalez-Aguilera C, Aguilera A (2008) Biogenesis of mRNPs: integrating different processes in the eukaryotic nucleus. Chromosoma 117: 319–331. doi: 10.1007/s00412-008-0158-4 18427828

68. Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, et al. (2003) FACT facilitates transcription-dependent nucleosome alteration. Science 301: 1090–1093. 12934006

69. Jin J, Cai Y, Yao T, Gottschalk AJ, Florens L, et al. (2005) A mammalian chromatin remodeling complex with similarities to the yeast INO80 complex. J Biol Chem 280: 41207–41212. 16230350

70. Tong JK, Hassig CA, Schnitzler GR, Kingston RE, Schreiber SL (1998) Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex. Nature 395: 917–921. 9804427

71. Ozturk N, Singh I, Mehta A, Braun T, Barreto G (2014) HMGA proteins as modulators of chromatin structure during transcriptional activation. Front Cell Dev Biol 2: 5. doi: 10.3389/fcell.2014.00005 25364713

72. Wu S, Shi Y, Mulligan P, Gay F, Landry J, et al. (2007) A YY1-INO80 complex regulates genomic stability through homologous recombination-based repair. Nat Struct Mol Biol 14: 1165–1172. 18026119

73. Oliveira DV, Kato A, Nakamura K, Ikura T, Okada M, et al. (2014) Histone chaperone FACT regulates homologous recombination by chromatin remodeling through interaction with RNF20. J Cell Sci 127: 763–772. doi: 10.1242/jcs.135855 24357716

74. Carrozza MJ, DeLuca N (1998) The high mobility group protein 1 is a coactivator of herpes simplex virus ICP4 in vitro. J Virol 72: 6752–6757. 9658123

75. Kettenberger H, Armache KJ, Cramer P (2003) Architecture of the RNA polymerase II-TFIIS complex and implications for mRNA cleavage. Cell 114: 347–357. 12914699

76. Kwak H, Lis JT (2013) Control of transcriptional elongation. Annu Rev Genet 47: 483–508. doi: 10.1146/annurev-genet-110711-155440 24050178

77. Bunch H, Zheng X, Burkholder A, Dillon ST, Motola S, et al. (2014) TRIM28 regulates RNA polymerase II promoter-proximal pausing and pause release. Nat Struct Mol Biol 21: 876–883. doi: 10.1038/nsmb.2878 25173174

78. Roy AL, Meisterernst M, Pognonec P, Roeder RG (1991) Cooperative interaction of an initiator-binding transcription initiation factor and the helix-loop-helix activator USF. Nature 354: 245–248. 1961251

79. Leopardi R, Ward PL, Ogle WO, Roizman B (1997) Association of herpes simplex virus regulatory protein ICP22 with transcriptional complexes containing EAP, ICP4, RNA polymerase II, and viral DNA requires posttranslational modification by the U(L)13 proteinkinase. J Virol 71: 1133–1139. 8995634

80. Lin FS, Ding Q, Guo H, Zheng AC (2010) The herpes simplex virus type 1 infected cell protein 22. Virol Sin 25: 1–7. doi: 10.1007/s12250-010-3080-x 20960278

81. Gierasch WW, Zimmerman DL, Ward SL, Vanheyningen TK, Romine JD, et al. (2006) Construction and characterization of bacterial artificial chromosomes containing HSV-1 strains 17 and KOS. J Virol Methods 135: 197–206. 16647145

82. Tischer BK, von Einem J, Kaufer B, Osterrieder N (2006) Two-step red-mediated recombination for versatile high-efficiency markerless DNA manipulation in Escherichia coli. Biotechniques 40: 191–197. 16526409

83. Tischer BK, Smith GA, Osterrieder N (2010) En passant mutagenesis: a two step markerless red recombination system. Methods Mol Biol 634: 421–430. doi: 10.1007/978-1-60761-652-8_30 20677001

84. Samaniego LA, Webb AL, DeLuca NA (1995) Functional interactions between herpes simplex virus immediate-early proteins during infection: gene expression as a consequence of ICP27 and different domains of ICP4. J Virol 69: 5705–5715. 7637016

85. Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98: 503–517. 1195397

86. Wagner LM, Lester JT, Sivrich FL, DeLuca NA (2012) The N terminus and C terminus of herpes simplex virus 1 ICP4 cooperate to activate viral gene expression. J Virol 86: 6862–6874. doi: 10.1128/JVI.00651-12 22496239

87. Gokhale A, Larimore J, Werner E, So L, Moreno-De-Luca A, et al. (2012) Quantitative proteomic and genetic analyses of the schizophrenia susceptibility factor dysbindin identify novel roles of the biogenesis of lysosome-related organelles complex 1. J Neurosci 32: 3697–3711. doi: 10.1523/JNEUROSCI.5640-11.2012 22423091

88. Harkness JM, Kader M, DeLuca NA (2014) Transcription of the herpes simplex virus 1 genome during productive and quiescent infection of neuronal and nonneuronal cells. J Virol 88: 6847–6861. doi: 10.1128/JVI.00516-14 24719411